Revista de Biología Tropical ISSN: 0034-7744 [email protected] Universidad de Costa Rica Costa Rica

Anelie Guimarães, Diva; Mitio Ohashi, Otávio; Singh, Michele; Vale, William Profile of plasmatic progesterone on pregnancy, and the postpartum estrus of Dasyprocta prymnolopha (Rodentia: ) Revista de Biología Tropical, vol. 64, núm. 4, 2016, pp. 1-8 Universidad de Costa Rica San Pedro de Montes de Oca, Costa Rica

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Diva Anelie Guimarães1, Otávio Mitio Ohashi1, Michele Singh2 & William Vale3 1. Institute of Biological Sciences, Federal University of Pará. Rua Augusto Corrêa 1, Guamá, Belém, Estado do Pará, CEP 66075-110, ; [email protected], [email protected] 2. Faculty of Food and Agriculture, Department of Food Production, The University of the West Indies. St. Augustine, Trinidad and Tobago, West Indies; [email protected] 3. Institute of Science and Technology of Water, Federal University of Western Pará. Rua Vera Paz s/n (Unidade Tapajós), Salé, CEP 68035-110, Santarém, Estado do Pará, Brazil; [email protected]

Received 23-IX-2015. Corrected 06-V-2016. Accepted 07-VI-2016.

Abstract: The (Dasyprocta sp.) is a hystricomorph found in some regions of the Americas. It is an important cynegetic , which indicates that the overhunting is a threat to their conservation. Very little is known about this wildlife in relation to what already has been studied in domestic . Thus, the knowledge on reproduction of wildlife becomes necessary and essential for the management and conservation of these natural resources. Specifically, studies regarding hormonal monitoring are important as a basic tool for research in modern reproductive biotechnology, and currently, there is no information on the progesterone changes during pregnancy of Dasyprocta sp., compared to other hystricomorphs. The aim of this study was to describe the profile of plasmatic progesterone during pregnancy, and report the restart of ovarian cycle in agouti after parturition. For this purpose, 18 black-rumped (Dasyprocta prymnolopha) born in captivity were used, and one or more consecutive pregnancies were observed. Copulation was confirmed by the presence of spermatozoa observed in the colpocytological examination. Blood samples were collected two times per week, and concentrations of progesterone, assessed in ten agoutis, were determined by radioimmunoassay. The onset of ovarian activity in six females was observed daily by colpocytological examination, starting on the seventh day postpartum. The gestational period observed in this study was 104.04 days (SD = 1.31) (101-106 days) (Number of cases, N = 26), and the interval between births was 126.03 days (SD = 18.40) (109-184 days). The plasmatic profile of progesterone during pregnancy showed a progressive increase from the 1st to the 5th week. The higher progesterone levels over this period (6.88 ng / mL, SD = 3.01) were detected in the 5th week. This value was similar (One-Way ANOVA, p > 0.05) to that observed in the 4th and 6th weeks, but was statistically different (One-Way ANOVA, p < 0.05) when compared to the other weeks. After the 6th week there was a progressive decrease in plasmatic progesterone levels. The animals showed a postpartum estrus of 12.04 days (SD= 4.29) (7-24 days) (N= 23). It was observed that 80.95 % (N= 19) of copulations during this period were fertile. This work contributed to understanding the dynamic changes in the progesterone levels during the pregnancy in agou- ti. Nevertheless, more studies are needed for a better appreciation of other endocrine and biological changes, in the mother and feto-placental unit of the agouti. Rev. Biol. Trop. 64 (4): 000-000. Epub 2016 December 01.

Key words: hystricomorph, agouti, gestation, postpartum, progesterone.

The hystricomorph , such as paca in this region, makes the management of wild- (Cuniculus paca), agouti (Dasyprocta sp.) and life an essential tool for food sovereignty and other wild , serve as protein biodiversity conservation (Bonaudo, Le Pendu, sources for local rural communities (Valsecchi, Faure, & Quanz, 2005). El Bizri, & Figueira, 2014; Van Vliet et al., However, to achieve success in man- 2015), which usually leads to overhunting in agement of wild mammals, the study of its the Amazon. This socio-environmental impact reproductive biology is required (Andrabi &

Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 64 (4): 000-000, December 2016 1 Maxwell, 2007), since it is poorly understood Myocastor coypus, Erethizon dorsatum, Hystrix (Wildt & Wemmer, 1999; Fickel, Wagcher, & africaeaustralis, and Cuniculus paca (Row- Ludwig, 2007). Knowledge of reproductive lands, Tam, & Kleiman, 1970; Challis, Heap, physiology, through endocrine monitoring is & Illingworth, 1971; Tam, 1973; Louis, Somes, a key tool for animal husbandry practices, as Pryor, & Blankenship, 1986; Van Aarde & Pot- well as integrated studies in different areas, gieter, 1986; Jakubička, Barta, Nitray, & Sze- such as ethology and ecology (Pereira, 2007). leszczuková, 1989; Barta & Jakubička, 1991; Few reproductive techniques have been used Sweitzer & Holcombre, 1993; Van Wyk, Van for the management of wild animals, including Aarde, & Louw, 1994; Ribeiro et al., 2012). hormonal monitoring. Thus, all the technology Thus, the aim of this study was to describe the has value to generate new information for spe- changes in the levels of progesterone during cies which are poorly studied. When there is pregnancy, and report the restart of ovarian availability of basic data, such as knowledge cyclicity postpartum in agoutis. of reproductive hormones, it will be pos- sible to use modern biotechnology techniques MATERIAL AND METHODS (i.e. artificial insemination, embryo transfer, cryopreservation of gametes and intracytoplas- The black-rumped agoutis (Dasyprocta mic sperm injections, for genetic management prymnolopha) were born in captivity, at a and conservation of the species (Pukazhenthi, wildlife paddock of the Federal University of Comizzoli, Travis, & Wildt, 2006). Pará, Belém, Brazil (1º27’ 21” S - 48º30’ 14” Long gestation periods are observed in W). Each female was housed with a male in tropical mammals. Some authors suggest that breeding paddocks of 4 m2, with a concrete is due to adaptations to the environment more floor and roof, and under natural lighting and favorable to births, within a longer period of ambient temperature (28 ºC) conditions. Daily time (Kiltie, 1982), and others to the precocity food supply was composed of cob corn (Zea of their young (Martin & MacLarnon, 1985). In mays), soybean (Glycine hispida), pumpkin the suborder hystricomorph, this aspect would (Curcibita pepo), cassava (Manihot utilissima), be associated with slow fetal growth, especially mineral salt, water ad libitum, with oral admin- in the early embryological stages (Roberts, istration of a nutritional complement two times 1971). The gestation period in agouti is about a week (Potenay Oral NF - Fort Dodge Saúde three and a half months, giving birth to two pre- Animal LTDA, Brazil), using a veterinary oral cocial young (Brown, 1936; Roth-Kolar, 1957; dosing syringe (M68 syringes for vermifuga- Nieuwendijk, 1980; Sousa et al., 2012; Fortes tion - Aparelhos veterinários Höppner LTDA, et al., 2013). The corpus luteum synthesizes Brazil). The protocol of this experiment was progesterone during the first weeks of preg- carried out in accordance with the Guide for the nancy in hystricomorphs and then the placenta care and use of laboratory animals (National performs this function (Tam, 1970, 1974). Research Council, 2011). In this suborder, the beginning of pregnancy A total of 18 adult females of agouti aged is characterized by low progesterone levels more than 24 months, and weighing 2 kg on compared to more advanced stages. After this average, were selected. Each female was kept period, there is a progressive increase in the in their respective breeding paddocks (4 m2). hormone levels, which gradually decrease near One or more consecutive pregnancies were parturition (Tam, 1974). observed in each female. Copulation was con- In the literature, there is no information on firmed by the presence of spermatozoa in the the progesterone changes during the pregnancy colpocytological examination, and day zero of Dasyprocta sp., compared to other hystrico- corresponded to the day of mating. morph, such as Myoprocta pratti, Cavia porcel- Concentrations of plasmatic progesterone lus, Galea musteloides, Dolichotis patagonum, were determined only in ten agoutis. To avoid

2 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 64 (4): 000-000, December 2016 long periods of capture stress, the animals were Tukey’s test, was applied to analyze whether distributed into the following groups: 1- Five there were significant differences (p < 0.05) females were monitored from mating to the on hormonal levels during pregnancy; and 50th day of pregnancy; 2- Another five preg- between the number of suckled offspring and nant animals were monitored from day 50 to the postpartum estrus period. 6 hours after delivery. The blood samples (0.5 mL) were collected RESULTS two times per week (72 and 96 hours intervals) (Van Aarde & Potgieter, 1986), by saphenous The average gestational period observed in venipuncture, without sedation. A total of 15 this study was 104.04 (SD= 1.31) days, with a samples were taken from each female. A 1 mL range of 101-106 days (Number of cases, N= syringe with 26 ½-gauge needle (Baas, Potkay, 26, 78.79 %), and a birth interval of 126.03 & Bacher, 1976), containing sodium heparin days (SD= 18.40) (range of 109 - 184 days). (Liquemine-Roche, Brazil) was used. After The plasmatic profile of progesterone dur- collection, the blood was put into a polypro- ing pregnancy showed a progressive increase pylene tube and immediately centrifuged at from the 1st to the 5th week. The higher hor- 1 000 revolutions per minute for 10 minutes. mone levels over this period (6.88 ng / mL, The plasma was stored at - 20 ºC until assayed. SD= 3.01) were detected in the 5th week (29th The progesterone was measured by radio- to the 35th day). This value was similar (One- immunoassay I125 in the solid phase (Diag- Way ANOVA, p > 0.05) to that observed in the nostic Products Corporation, USA). The assay 4th and 6th weeks, but was statistically different quality control samples, containing high and (One - Way ANOVA, p < 0.05) when com- low hormone concentrations, were included pared to the other weeks. After the 6th week at the beginning and the end of each assay. there was a progressive decrease in plasmatic Coefficient variations of intra-assay and inter- progesterone levels. From the 7th week until assay were 11 % and 10 %, respectively. The delivery, there was no statistical difference specificity of the assay for progesterone was (One - Way ANOVA, p > 0.05) in the levels of 100 % (17-hydroxyprogesterone 0.3 %; 20 this hormone (Fig. 1). a-dihydroprogesterone: 2.0 %), and the sensi- The following gestational problems (N= tivity was 0.02 ng / mL. 7, 21.21 %) were observed: 1- embryonic After delivery, the onset of ovarian activity death after 46 days and 50 days of pregnancy in six females was observed daily by colpocy- (N= 2), verified by the decrease in the levels tological examination, starting at the seventh of progesterone (Fig. 2); 2- abortions at 73 day postpartum. Copulation was confirmed days and 84 days of gestation (N= 2) (Fig. 2); by the observation of sperm in the vaginal 3- post-term delivery (106 days, 108 days and smear. The postpartum period was monitored 110 days), with consequent dystocia, that result four times in five females, and three times in complicated birthing (N= 3). No perinatal in one animal, until copulation. The clinical mortalities were observed. examination for pregnancy diagnosis (abdomi- The animals showed a postpartum estrus nal palpation, auscultation and observation of on average of 12.04 days (SD= 4.29) (7-24 breast development) was conducted on the 40th days) (N= 23). It was observed that 80.95 % day after copulation. (N= 19) of copulations during this period were Statistical analyses were performed using fertile, with the subsequent birth of a young. SPSS/PC (IBM, USA). Values were expressed The gestational period was not confirmed in as the mean and Standard Deviation (SD). 9.52 % (N= 2) females showing postpartum The level of significance throughout the study estrus, although copulation was observed. No was 0.05 (p < 0.05). Analysis of variance mating was observed in two other animals (One-Way ANOVA), in conjunction with displaying postpartum estrus. The number

Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 64 (4): 000-000, December 2016 3 8

7

6

5

4 P4 (ng / mL) 3

2

1

0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 Weeks of pregnancy Mating Parturition

Fig. 1. Mean plasmatic concentrations of progesterone during pregnancy period in agoutis (N = 10).

14

12

10

8

P4 (ng / mL) 6

4

2

0 0 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75 80 Days of pregnancy

Fig. 2. Decreases in the plasmatic levels of progesterone in agouti, associated to fetal death on the 46th day of pregnancy (dashed line) or to abortion during the 84th day of gestation (solid line).

4 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 64 (4): 000-000, December 2016 of suckled offspring (1-3) had no influence (Louis et al., 1986), which showed elevated th on the postpartum estrus period (One-Way levels of progesterone after the 4 week (26th ANOVA, p > 0.05). day) of gestation, until the time of delivery. In M. coypus the highest levels of this hormone was observed between the 14th and 15th week DISCUSSION of gestation (12.5 to 20.72 ng / mL) (Jakubička The study of the profile of plasmatic pro- et al., 1989; Barta & Jakubička, 1991); and in th th gesterone during pregnancy is an important H. africaeaustralis between the 6 and 12 tool for diagnosis and prognosis of this period, week (202 ng / mL, SD= 98) of pregnancy targeting correct reproductive management. (Van Aarde & Potgieter, 1986; Van Wyk et al., Moreover, this knowledge is fundamental and 1994). However, during early and mid-preg- necessary to a better understanding of repro- nancy, the progesterone levels in agouti were ductive physiology of wild animals, which is similar to those found in E. dorsatum (4 ng / still very poorly studied. mL) (Sweitzer & Holcombre, 1993), and to the When compared to other rodent suborders, maximum values observed after the 60th and 9th the hystricomorphs such as the agouti show a days of gestation in C. paca (3.03 ng / mL and long period of gestation (Weir, 1974). This fea- 3.55 ng / mL) (Ribeiro et al., 2012). ture could be related to the birth of precocious The ovary of pregnant agouti has function- individuals, adapted to rapid growth and low al (N= 2) and accessory corpora lutea, required parental investment. On these aspects, Lange, for continuous production of hormones (Mayor, Abilhôa, Margarido and Monteiro Filho (2003) Bodmer & López-Bejar, 2011). In general, the stated that the offspring of agoutis (D. azarae), synthesis of progesterone in hystricomorphs from larger (lighter) and smaller (heavier) lit- rodents, during the first stage of pregnancy, ters, have a similar growth potential, attained at occurs in the corpus luteum. After this period, six months of age at approximate final weight. in C. porcellus and G. musteloides, the placenta Furthermore, these animals are already able, is responsible for progesterone supplementa- from the first days of life, to consume solid tion (Tam, 1970, 1974). The period between the food, suggesting their autonomy. 4th and 6th week of gestation in agouti, when the The initial stage of pregnancy in agouti is progesterone levels are higher, corresponds to characterized by the progressively increasing the rapid development of the primordial brain progesterone levels until the sixth week. Sub- vesicle (25th to 30th day of gestation) (Fortes et sequently, the concentration of this hormone al., 2013); the first detection of the embryo (18 declined until delivery. This secretion pattern to 22 days of gestation), fetal heartbeat (25th is similar to that proposed by Tam (1974) day of gestation) by ultrasound and the visibil- for hystricomorphs. ity of the placenta (day 21 of gestation) (Sousa Despite the similarity in the secretory et al., 2012). In relation to this endocrine organ, pattern, the levels of progesterone observed there is a gradual increase up to the 60th day in agouti were lower than those found in M. of gestation, after which regression begins pratti (50 ng / mL) (Rowlands et al., 1970); C. (Sousa et al., 2012). This period coincides with porcellus (15 ng / mL in the 15th day of gesta- the lowest levels of progesterone observed tion; 329 ng / mL (SD= 14) between the 30th in the present study occurring during the last and 45th day; 160 ng / mL (SD= 14), between gestational stage. 51th and 55th days) (Challis et al., 1971); and The progressive increase in the plasmatic G. musteloides (23 to 60 ng / mL in 15th day of levels of progesterone until the 6th week in gestation; 513 ng / mL in 26th day; 108 ng / mL agouti shows the great importance of luteal a few days before delivery) (Tam, 1973). More- secretion in the maintenance of the endome- over, this model of progesterone synthesis was trium and consequent embryo development different from that observed in D. patagonum during the early pregnancy. This suggests that

Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 64 (4): 000-000, December 2016 5 from the middle of this period, the placenta long in the hystricomorphs, the fertile postpar- might play a more active role in the gestation tum estrus could ensure a rapid replacement of this species. This possibility can be verified of the population size. in the guinea pig (C. porcellus), as ovariectomy In conclusion, this work contributed to performed after the middle of this period, does understand the dynamic changes in proges- not cause abortion, due to sufficient progester- terone levels during the pregnancy in agouti, one produced by the placenta (Hafez, 1980). comparing it to other hystricomorphs and asso- Concerning embryonic death and abor- ciating it to the main events of embryonic tion observed in this study, it is possible that development of this species. This represents a endocrine disorders related to maternal age scientific advancement for future implementa- have occurred, as it was the first pregnancy for tion of reproductive biotechnologies that aim at young females. According to Jainudeen and conservation of this species. On the other hand, Hafez (2004), the causes of prenatal mortality the agouti has a long gestation period, with may be due to fetal or maternal factors (eg. rapid onset of a fertile postpartum estrus, and genetic, endocrine, nutritional, age). Further- produces precocious young, indicating that is a more, in domestic animals, around 25 to 40 promising species for zootechnical production. % of the embryos are usually lost. It was not However, further investigations are needed to possible to clarify the cause of post - term study other endocrine and biological changes pregnancy observed in this work. However, in the maternal and feto-placental unit of the these problems are generally due to fetopel- agouti, in an attempt to better understand the vic disproportion, abnormal feto positions, reproductive failures observed in these animals. absence of uterine contraction, and others. The reproductive failure problems observed ACKNOWLEDGMENTS in this study were considered as idiopathic causes. Therefore, more studies are necessary We thank the Federal University of Pará, for further information. their technicians for assistance in collecting Agoutis have a postpartum estrus of an materials for this research and the International average of 12.4 days, which corroborates with Foundation for Science (Ref. B/2659-1) for Weir (1971). Considering the fertilization rate supporting this project. The authors thank of 85 % to 100 %, for the species which con- Martín Alvarez for his help in translation of the ceive more than one young (McDonald, 1980), abstract into Spanish. and the observation that 80.95 % of copula- tions occurred during the postpartum period preceding the normal pregnancies in the agouti, RESUMEN it can be stated that this species is relatively Perfil de la progesterona plasmática durante fertile in this period. Similarly, many hystri- durante la preñez y celo posparto del Dasyprocta prym- comorphs exhibit postpartum estrus. However, nolopha (Rodentia: Dasyproctidae). El agouti (Dasyproc- in C. porcellus, G. musteloides, M. coypus and ta sp.) es un roedor histricomorfo encontrado en algunas Chinchilla laniger, copulation in postpartum is regiones de América. Es una especie cinegética importante, not always fertile, even though mating of these lo que indica que la caza excesiva es una amenaza para su conservación. Muy poco es lo que se conoce acerca de la species has been observed during this period biología de los animales silvestres, en relación al conoci- (Weir, 1970, 1973, 1974; Roberts, Maliniak miento acumulado sobre los domésticos. Por lo tanto, el & Deal, 1984; Roberts, Koontz, Phillips & estudio sobre la reproducción de los animales silvestres se Maliniak, 1987; Iwata, 1989; Jarvis, 1991; hace necesario e imprescindible para el manejo y conser- Jori, 1998). The presence of postpartum estrus vación de la especie como recurso natural. En concreto, los estudios relativos a la monitorización hormonal son and the subsequent development of another una herramienta básica para la investigación en biotecno- pregnancy in agouti is a positive factor for logía reproductiva moderna. No hay información sobre los this species. Because the gestation period is cambios de progesterona durante la preñez de Dasyprocta

6 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 64 (4): 000-000, December 2016 sp. en comparación con otros histricomorfos. El objetivo Brown, C. E. (1936). Rearing wild animals in captivity, and de este estudio fue describir el perfil de la progesterona gestation periods. Journal of Mammalogy, 17, 10-13. plasmática durante la preñez, y reportar el reinicio del Challis, J. R. G., Heap, R. B., & Illingworth, D. V. ciclo ovárico después del parto. Para ello, se utilizaron 18 (1971). Concentrations of estrogen and progesterone agoutis de rabo negro (Dasyprocta prymnolopha) nacidos in the plasma of non-pregnant, pregnant and lactating en cautiverio. Fueron estudiadas una o más preñeces conse- guinea-pigs. Journal of Endocrinology, 51, 333-345. cutivas. La copulación fue confirmada por la presencia de espermatozoides observados en examen colpocitológico. Fickel, J., Wagcher, A., & Ludwig, A. (2007). Semen Las muestras de sangre se recogieron dos veces por sema- cryopreservation and the conservation of endangered na, y las concentraciones de progesterona se determinaron species. European Journal of Wildlife Research, 53, 81-89. en 10 individuos mediante radioinmunoensayo. Se observó el inicio de la actividad ovárica diaria por examen colpoci- Fortes, E. A., Ferraz, M. S., Bezerra, D. O., Júnior, A. tológico, comenzando en el día séptimo posparto. El perío- M., Cabral, R. M., Sousa, F. D., … Carvalho, M. A. do gestacional observado en este estudio fue de 104.04 días (2013). Prenatal development of the agouti (Dasy- (SD= 1.31, rango entre 101-106 días, N= 26), y el intervalo procta prymnolopha, Wagler, 1831): External featu- entre los nacimientos fue 126.03 días (SD= 18.40, rango res and growth curves. Animal Reproduction Science, entre 109-184 días). El perfil plasmático de la progesterona 140(3-4), 195-205. durante el embarazo mostró un aumento progresivo de la 1ª Hafez, E. S. E. (1980). Laboratory animals. In E. S. E. a la 5ª semana. Los mayores niveles de progesterona duran- Hafez (Ed.), Reproduction in farm animals (pp. 409- te este período (6.88 ng / mL, SD= 3.01) se detectaron en 422). Philadelphia, USA: Lea & Febiger. la quinta semana. Este valor fue similar (ANOVA de um factor, p > 0.05) al observado en las semanas cuatro y seis, Iwata, K. (1989). Breeding physiology of pacarana pero fue estadísticamente diferente (ANOVA de um factor, Dinomys branickii. Journal Japanese Association of Zoological Gardens and Aquariums, 31(2), 47-50. p<0.05) en comparación con las otras semanas. Después de la sexta semana hubo una disminución progresiva en los Jainudeen, M. R., & Hafez, E. S. E. (2004). Falha niveles plasmáticos de progesterona. Los animales mostra- reprodutiva em fêmea. In B. Hafez & E. S. E. ron un estro posparto de 12.04 días (SD= 4.29, rango entre Hafez (Eds.), Reprodução animal (pp. 261-278). São 7-24 días, N= 23). Se observó que el 80.95 % (N= 19) de Paulo, Brasil: Manole. cópulas durante este período fueron fértiles. Este trabajo contribuyó a la comprensión de los cambios dinámicos en Jakubička, I., Barta, M., Nitray, J., & Szeleszczuková, O. (1989). Fluctuations in the concentration of progeste- los niveles de progesterona durante la preñez del agouti. rone in the peripheral blood of coypus during gravi- Sin embargo, se necesitan más estudios para una mejor dity. Veterinarni Medicina (Praha), 34(4), 251-256. comprensión de otros cambios biológicos y endocrinos, y en la unidad materna y feto-placentaria del agouti. Jori, F. (1998). Anatomía funcional del aparato repro- ductor femenino del puerco espín de cola de pincel Palabras clave: histricomorfos, agouti, gestación, pospar- (Atherurus africanus) (Doctoral Dissertation). Uni- versitat Autónoma de Barcelona, Spain. to, progesterona. Jarvis, J. U. M. (1991). Reproduction of naked mole-rats. In P. W. Sherman, J. U. Jarvis, & R. D. Alexander REFERENCES (Eds.), The biology of the naked mole-rats (pp. 384- 425). New York, USA: Princeton University Press. Andrabi, S. M. H., & Maxwell, W. M. C. (2007). A review on reproductive biotechnologies for conservation of Kiltie, R. A. (1982). Intraspecific variation in the mam- endangered mammalian species. Animal Reproduc- malian gestation period. Journal of Mammalogy, tion Science, 99, 223-243. 63(4), 646-652.

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